Natural variation of radionuclide 1 3 7 ~ s

MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
Vol. 160: 109-120.1997
Published December IS
Natural variation of radionuclide 1 3 7 concentration
~s
in marine organisms with special reference to the
effect of food habits and trophic level
Fujio Kasamatsu*,Yusuke Ishikawa
Marine Ecology Research Institute, Tokyo Head Office, Teikoku Shoin Bldg, 3-29 Jinbo-cho, Kanda, Chiyoda, Tokyo 101, Japan
ABSTRACT. Although a number of measurements have been made on radiocesium concentrations in
aquatic organisms, no clear agreement has been reached on the factors affecting accumulation of these
radionuclides. Natural variations in the concentration of the long-lived artificial radionuclide '37Cs in
marine organisms and factors affecting variations in marine fishes were investigated through long-term
and systematic measurements in coastal waters of Japan from 1984 to 1995. Concentrations of 13'Cs
were measured in more than 30 species of crustaceans, cephalopods and teleosts considered representative of the marine biotic community. A clear positive correlation (p < 0.05) was found between mean
weight and concentration of 137Csin 276 fish samples. However, different relationships between 137Cs
concentration and weight of fish were observed in different species. Within 16 studied species I3'cs
concentration increased with growth for 4 species, while no specific correlation was observed in the
remaining species. These different patterns depended on a change of food habits with growth. Analysis of 6066 stomach contents of fish samples together with '37Csconcentrations in the stomach contents
demonstrated that 137Csconcentration increased with rising trophic level and that the biomagnification
factor (13'cs in p r e d a t ~ r / ' ~ ~in
C sprey) was 2.0 (95% confidence interval 1.8 to 2.2). From the yearly
change of '37Cs in 24 marine fish species, a mean effectlve environmental half-life of I3'Cs of 13 * 3 yr
(range 10 to 17 yr) was calculated.
KEY WORDS: Trophic level . Food habits . Marine
dependence . Environmental half-life
INTRODUCTION
The long-lived artificial radionuclide 137Cscan be
considered to be of great interest and importance as an
indicator of radioactive pollution in the marine environment because of its relatively high radiotoxicity. Its
major sources are the atmospheric deposition of debris
from past nuclear explosions during 1954 to 1962 and
1980. The nuclear accident at the Chernobyl nuclear
power station has renewed interest in this radionuclide.
The fate and cycling of radionuclides in ecosystems
have long been a subject of major interest to applied
ecologists and health physicists. Although many mea-
O Inter-Research 1997
Resale of full article not permitted
organisms
. Bioaccumulation . I3'Cs
,
Size-
surements have been made on radiocesium concentrations and their variations in aquatic organisms (e.g.
Williams & Pickering 1961, Baptist & Price 1962,
Hiyama & Shimizu 1964, King 1964, Morgan 1964,
Hasanen et al. 1968, Kolehmainen et al. 1968, Jefferies
& Hewett 1971, Pentreath & Jefferies 1971, Whicker et
al. 1972, Pentreath 1973, Suzuki et al. 1973, Newman &
Brisbin 1990, Tateda & Misonou 1991, Morgan et al.
1993, Cocchio et al. 1995),no agreement seems to have
been reached on the factors affecting the accumulation
of this radionuclide, and this lack of ecological understanding has hindered the development of a robust
dose model (Rowan & Rasmussen 1994).
Furthermore, the bioaccun~ulationof radionuclides
by aquatic organisms and the factors affecting the concentrations have been examined mainly under controlled conditions in aquaria. Such studies have been
110
Mar Ecol Prog Ser 160: 109-120, 1997
conducted on a limited range of marine species (generally species easy to rear in laboratory expenments) and
performed under conditions that cannot be truly representative of the natural environment. There have been
few direct and large-scale environmental studies on
'37Csaccumulation in marine organisms in the natural
environment.
Although there is a general agreement that food is
the major route of I3'Cs uptake by fish, some authors
claim varying degrees of biomagnification (Gustafson
1967), some deny food-chain effects (Reichle et al.
1970, Thomann 1981), and some even claim that the
radiocesium undergoes 'biodiminution' in aquatic food
chains (Mailhot et al. 1988).
The Marine Ecology Research Institute, Tokyo, has
been carrying out large-scale and systematic measurements of '37Cs concentrations of sea water, sediments
and marine edible organisms sampled from fishing
grounds along the coast of Japan since 1984 as part
of a n extended marine environmental radioactive
monitoring program sponsored by the Science and
Technology Agency of Japan. This paper reports the
variation of '37Csin edible marine organisms, with special reference to the factors affecting 13?Csconcentration, based on results from the long-term measurements at different locations around Japan over more
than 10 yr (1984 to 1995).
24 h. Samples were analyzed using Gamma-spectrometry to determine 137Cs(measuring for 20 h ) . Results
were expressed as Bq kg-' wet weight for I3?Cs.
13?cs concentrations in sea water were measured
from 50 1 samples. Cesium was absorbed onto ammonium molybdophosphate precipitate under acidic conditions, and 137Cswas separated by means of a cation
exchange resin column method, fixed as cesium chloroplatinate and measured by Gamma-spectrometry
(measuring for 20 h). Food habits of the studied fish
species were investigated from their stomach contents.
Stomach contents were expressed as a percentage of
weight of each prey item against total weight of stomach contents.
RESULTS
Variation oi 13'Cs concen1ra:ions in marine organisms
Table 1 shows details of the marine organisms analyzed from 1984 to 1995, together with their concentrations of 137Csand mean concentration factors (CF; concentration in organism/concentration in sea water) of
13'Cs during the years 1992 to 1995. Tables 2 & 3 shows
MATERIALS AND METHODS
Sampling areas and samples. The locations of sampling sites are shown in Fig. 1. For the purpose of the
monitoring program, marine organisms to be analyzed
were selected from coastal species which have been
abundantly caught by the coastal fisheries of Japan.
Marine organism samples were taken on the continental shelf and shelf slope (between the sea surface and
approximately 500 m depth) around Japan, through
various fishing operations. These samples were provided twice a year by the local fisherman's union. Samples of marine organisms were frozen and transferred
to the laboratory. More than 30 species (representing
more than 20 families) of marine organisms were sampled. The samples consisted of teleosts, cephalopods
and crustaceans. The species and samples measured
during 1984 to 1995 are shown in Table 1. Sea water
was sampled once a year using a Niskin type bottle,
taking 80 1 per sample.
Measurement. Samples of marine organisms (total
wet weight about 20 kg) were transported to the Japan
Chemical Analysis Center, where the major part of the
analysis was carried out. Muscle tissues from each fish
were dissected out and pooled. After being dried at
105"C, individual samples were ashed at 450°C for
P4ClFlC OCEAN
'W
Kagoshi ma
0Sampling area for organisms samples
Sarnpl~ngsrarion for sea warer samples
Nuclear power plant
Fig. 1. Sampling sites in Japan
Kasamatsu & Ishikawa: '37Csconcentrations In m a n n e organisms
111
:able 1. Length, wet welght and concentration of '"CS in marine organisms measured during 1984 to 1995. CF: concentration facor (concentration in organism/concentration in sea water). ND: not detected; concentration less than 3 times the analysis errors
Species
Chondrichthyes
Order Rajiformes
Family Dasyatididae
Stingrays
Osteichthyes
Order Anguiliformes
Family Congridae
Common Japanese conger
Order Salmon~formes
Family Argentlnldae
Deep-sea smelt
Order Gadlformes
Family Mondae
Mond cod
Family Gadidae
Pacific cod
Walleye pollack
Order Scorpaeniformes
Family Scorpaenidae
Scorpion fish
Black rockfish
Family Platycephalidae
Bertail flathead
Family Hexagrammldae
Atka mackerel
Greenling
Order Perciformes
Family Perc~chthyidae
Japanese sea bass
Family Carangidae
Jacks
Family Spandae
Red sea bream
Crimson sea bream
Yellow sea bream
Family Sciaenidae
White croaker
Black mouth croak
Family Girellidae
Rudder fish
Family Trichodontidae
Japanese sandfish
Order Pleuronectiforms
Family Paralichthyidae
Bastard halibut
Family Pleuronectidae
Flathead flounder
Pointhead flounder
Shothole halibut
Stone flounder
Brown sole
Marbled sole
Rikuzen sole
Family Cynogloss~dae
Black tonguefish
Red tonguef~sh
Cephalopods
Family Decapoda
Family Octopoda
Crustacea
Family Decapoda
No. of
samples
Mean length
Max. Min.
(cm)
Mean wet weight
Max. Min.
(g)
Concentration
Max. Min.
(Bq kg-' fresh)
Mean
C F & SD
1992-95
112
Mar Ecol Prog Ser 160: 109-120, 1997
--
mean concentrations of '"CS in sea water (0 to 200 m
depth) during the period 1984 to 1995 (14 sites with
56 stations) and '"'CS in sea water by depth (1992 to
1995), respectively.
Concentration of I3'Cs in fishes ranged from 0.05 to
0.74 Bq kg-' fresh wt ( n = 746) during 1984 to 1995 and
the 1992-95 overall mean concentration factor was 59 +
24 (n = 276). Concentration of 137Csin squids varied
from ND (not detected) to 0.09 Bq kg-' fresh wt (n = 53),
and that of octopus from ND to 0.09 Bq kg-' fresh wt
(n = 89). Concentration of '37Csin shrimps (Crustacea
Decapoda) ranged from 0.04 to 0.19 Bq kg-' fresh wt
(n = 23) with 1992-1995 mean CF of 26 + 10 ( n = 31).
Table 2. Mean concentrations of ' " ~ C S in the coastal surface
sea water ( 0 to 200 m depth)
Year
'"CS SD
(mBq I-')
No. of
samples
Sampl~ng
penod
Mar-Dec
Jun-Aug
May-Jul
May-Rug
May-Jul
May-Jul
May-Jul
May-Jul
May-Jul
May-Jun
May-Jul
May-Jul
Effect of a r e a on '37Cs concentration
The possible effect of area of origin on the concentrations of '"CS was investigated by comparing concentrations by areas and by species (Table 4 ) .
Table 3 . Mean concentrations of '"'CS of sea water by depth in
There were no significant differences in the concencoastal waters during 1992 to 1995
trations between areas except in 2 species, Atka mackerel Pleurogrammus azonus and common Japanese
Depth
:17cS
SD
No. of
conger Conger myriaster. There was no difference in
(m)
(mBq I-')
samples
the depth of habitats and the I3'Cs concentrations of
0-200
3.15
0.35
416
the sea waters between the areas (Kasamatsu & Inatom
34
200-300
2.75
0.57
1997). In the case of the common Japanese conger,
300-400
2.42
0.40
24
however, a large difference in size between areas was
400-520
1.90
0.33
23
noted. The concentration of "'CS in this species is sizedependent (as discussed in the following section). A possible reason for the
difference in '37Cs concentration in
Table 4. Mean concentration factors of '"CS in 7 species from different areas.
CF: concentration factor
Atka mackerel between areas is also
explained in the 'Discussion'.
Effect of fish size on 13'Cs
concentration
Fig. 2 shows the relationship between mean CF of '37Csand the mean
total length and the mean body weight
for 28 fish species (147 samples)
obtained during 1992 to 1.995. There
was a clear positive correl.ation (the
slopes are significantly different from
zero at 5 % level). This demonstrates
that the heavier and bigger species in
the marine fish community apparently
have the higher concentration factor
of '37Cs.
Fig. 3 shows the relationship between mean CF of I3'Cs and mean
body weight for the 14 major fish
species studied. Within these 14 spe-
Species
Sampling
area
I3'Cs
CF 2 SD
Walleye pollack
Hokkaido
Niigata
96 + 11
95 + 7
Japanese sea bass
Fukushima
Fukui
Saga
Bastard halibut
Hokkaido
lbaraki
Fukui
Shlmane
Atka mackerel
Hokkaido
Niigata
Japanese common
conger
Miyagi
Fu kui
Red sea bream
Shlmane
Fukui
Pacific cod
Miyagi
Fukushima
'Signif~cantlydifferent at 5'%,level, "at 1
No. of
samples
level
Mean
weight + S D (g)
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Mar Ecol Prog Ser 160: 109-120, 1997
s
In stomach contents. CF: concentration factor
Table 5. i ' i 7 ~concentrations
Stomach
contents
Flsh (large size)
F ~ s h(small SIX)
Fish (combined)
Crustacean Decapoda
Cephalopoda
Benthos
Zooplankton
1 ' ' 7 ~ s 4(CF)
( B q kg-']
*
0.15 0.01 (481
0.10 ? 0.01 (321
0.12 0.01 (38)
0.1 1 0.01 (35)
0.03 0.01 (10)
*
*
*
Major
contents
Horse mackerel etc.
Sandlance, anchovy etc,
Prawn, shrimp
Squid
Polychaetes
Euphausiacea
I3'Cs CF
from literatureh
56 * 24 (this work)
30 t 6 (11, (this work)
34 * 13 (i],(this work)
26 * 10 ( t h ~work)
s
17 ? 13 (iii]
4
8
*2
(11)
* 5-15 (I, iii)
dValues are shown i analysis error
"Literature.
(i) Ibaralu Environmental Pollution Research Center (1993, 1994, 1995);(ii)Pentreath & Jeffenes (1971);(iii) Gomez et al. (1991)
Fig. 4. Stomach contents and '37Cs concentrations of 20 fish
species. (H) Hokkaido;
(N) Niigata; (L) large;
(S) small
Kasamatsu & Ishikawa: I3'Cs concentrations
In
marine organisms
115
were observed in fish species whose prey was
large-size fishes (e.g. Japanese sea bass and
Pacific cod) and low concentrations were
observed in fish species whose prey was mainly
macro-benthos (e.g.brown sole and red tonguefish). It was, however, noted that relatively high
concentrations were observed in Atka mackerel, walleye pollack and deep-sea smelt Glossanodon semifasciata and that the food of these
fishes was not from the high trophic levels.
Fig. 5 shows stomach contents in relation to
body size (at different growth stages) for 9
major fish species. With increase of body size
(with growth) Pacific cod, stone flounder,
Japanese common conger and bertail flathead
apparently change their prey from that of low
trophic level to that of high trophic level. I3'Cs
in these species tends to increase with increase
in size. In contrast, within the examined range
of weight, flathead flounder, brown sole, Japanese sea bass and red sea bream do not change
their food habits. These observations suggested
that the size-dependent concentration of '37Cs is
mainly due to change of food habit.
A quantitative examination of the relationship
between the concentration of 1 3 7 ~ins food and
in fish was carried out. '37Cs in the intake-food
(I)is here expressed as follows:
where bi is the absorption percentage of 137Cs
for the ith food item,. di. is the concentration of
Crustacca l&Ccphal@
13'Cs in the ith food item (Table 5), and f , is the
Fish(L)
MacroFish(S)
bcnthos
proportion of the ith food item in the diet of fish
Fig. 5. Stomach contents of different body size ranges for the major
(Reichle 1969, Kolehmainen 1974). An absorp9 species
tion of 90% was assumed. Fig. 6 shows the relationship between '37Cs in the intake-food and
'37Cs in the fishes that inhabit surface layers (above
0.4
W fishes in surface lasers
approximately 150 m depth, closed circles in Fig. 6). A
0 fishes in dccprvalcr
significant positive relationship (r = 0.79, p < 0.001)
o
--, 0.3
was observed, suggesting food habits to be the major
0
factor affecting concentration of 137Csin fishes, and the
biomagnification factor (13'Cs in predator/13'Cs in
c
2
0.2 prey) was estimated at 2.0 (95% confidence interval
.-C
1.8 to 2.2).
m$;,On
g,ccapoda
-
/'
d
z-
0.1
-
m m
Effect of habitat on concentration
Fig. 7 shows depths of habitats and '"CS concentrations of 21 fish species samples. From the observations
presented in Figs. 6 & 7, it is noted that walleye pollack, ~ t k mackerel
a
and deep-sea smell that inhabit a
depth of 150 to 400 m with lower sea temperature have
high concentrations of '"CS despite low concentra-
y=ZOz:
O
.
0.00
O
j
-
.
0.05
CS in food (Bq/kg)
137
,
R' =0.63
,
I
0.10
~i~ 6, ~ ~ l ~of 13'~s
l ~concentration
~ ~ ~ between
h i foodr
~
and
fishes. ( 0 ) Fishes in surface layers, (0)fishes in deep-sea
waters (walleye pollack, Atka mackerel and deep-sea smelt)
Mar Ecol Prog Ser 160: 109-120, 1997
116
30 38 57 54 9:
Concentrat~onFactor
16 27 l ? 37 59 66 51 50 70 7 s 50 8C !? 73 76 94
weight were excluded to avoid sizedependent effects. The effective environmental half-lives range from 10
to 17 yr w ~ t ha mean of 13 + 3 yr
(Table 6). These half-l~ves were
slightly lower than those determined
in surface layers of sea water (16 to
18 yr; Kasamatsu & Inatomi 1997) but
not significantly different.
DISCUSSION
Flg 7 Depth of capture a n d I3'Cs concentration factors of the 21 fish species
studled Closed clrcles show depth of capture a n d vertlcal llnes show range of
depth from the literature Depths of captures were provlded from lntervlews
with fishermen conducted during 1994
Radiocesium '"CS falls to earth in a
readily soluble form following atomic
bomb detonations and is thus available to human beings through concentration and transfer up the food
chain. Identification of factors affecting or controlling accumulations of
13?Cs in edible marlne organisms is
critically necessary to identify pathways of radiocesium accumulation
from a surface input.
Factors affecting accumulation of
I3jCs in fishes have been the subject of
previous investigations (Bryan 1963,
tions in their food and in environmental sea water (see
Table 3).
Concentration factors along trophic level
L
Our investigations indicated that food habit was one
of the most important factors affecting concentrations
of 13'cs in m a n n e flshes, a n d Fig 8 shows the relationship between the 13jCs concentration factor and the
oceanic food chains A clear Increase in the concentration factor was observed with Increase In trophic level
Nevertheless most food relationships are not simple
food c h a ~ n sbut are more often complex as a result of
opportunistic feedlng I3jCs could be a good ind~cator
and/or a research tool for studies on food habits and
Fig. 9 shows the annual variation of '37Cs in 24 fish
specles after the Chernobyl accident (1987 to 1995).
The effective environmental half-lives were calculated
a n d the results a r e shown in Table 6. Species having
positive Or negative annual trends ln their mean body
weight or having a large yearly variation in mean body
Tclcosts
Species
Fig 8. ~~~d habits a n d mean Ii'cs concentration factors for
marine organisms. Vert~callines show standard dev~ation
Kasamatsu & Ishikawa: '."CS concentrations in marine organisms
-
--
00
!
1984
I
1986
117
-
1988
1990
1992
1994
1996
Year
Fig. 9. Yearly changes of mean concentrations of '"CS in 24
fish species. Lines are least squares fits to the data
1965, King 1964, Morgan 1964, Pendleton et al. 1965,
Hasanen et al. 1968, Kolehmainen et al. 1968, Pentreath 1973, Kasamatsu 1996). Morgan (1964),Hiyama
& Shimizu (1964), Morita (1980) and Yoshida (1992)
suggested a positive correlation between body size and
radiocesium concentration in fishes, while Hasanen &
Miettinen (1963), Kimura (1984), Newman & Brisbin
(1990), and Ishikawa et al. (1995) observed neither a
positive nor any other clear correlation between '17Cs
and size (or age) of fishes. However, the reason for this
discrepancy has not been clearly identified. We also
found both size-dependence and no size-dependence
of '37Cs concentration in different fish species. Our
analysis demonstrated that those different patterns
were due to changes of food habits with growth. The
I3?Cs concentration in the fish increased clearly when
the food habit changed from low trophic level to high
trophic level with growth, but it did not increase when
the fish did not change their prey. These results suggest
that food habit is one of the most important factors
affecting concentrations of 137Csin marine fishes.
The effect of food habits on '"CS concentration could
explain the difference in 13'Cs concentration in different areas (see Table 4). It has been suggested that the
difference of food of Atka mackerel from Hokkaido
(mainly fishes) and Niigata (mainly zooplankton)
might cause the difference in '"CS concentration
between areas, because zooplankton has a much lower
concentration of I3'Cs than fishes (Kasamatsu 1996).In
the case of common Japanese conger, size-dependent
concentration of '"'CS (Fig. 3) resulted in a high concentration in larger size fish (Fukui area) and a low
concentration in smaller size fish (Miyagi area). The
yearly variation of '"CS in stone flounders (Fig. 10)
before 1992 was well explained by the yearly variation
Table 6. Annual trends of '"'CS concentration in major fish species during 1987-1995
Species
Sloped
Halflife (yr)
Stingrays
Common Japanese conger ( M i y a g ~ )
Common Japanese conger (Fukui)
Deep-sea smelt
Pacific cod
Walleye pollack (Hokkaido)
Scorplon fish
Black rockflsh
Bertai.1 flathead
Atka mackerel (Hokkaido)
Japanese sea bass
Jacks
Red sea bream
Crimson sea bream
White croaker
Rudder fish
Japanese sandfish
Bastard halibut
Flathead flounder
Shothole halibut
Stone flounder
Brown sole
Black tonguefish
Red tonguefish
-0.045
-0.017
-0.049
-0.041
-0.092
-0.063
-0.053
-0.068
-0.052
-0.064
-0.075
-0.037
-0.079
-0.042
-0.052
-0.081
-0.055
-0.061
-0.063
-0.041
-0.078
-0.072
-0.057
-0.063
15 4
40 7
14 1
16.9
7.5
11.O
13.6
10 2
13 8
10.8
92
18.7
8.8
16.5
13.3
8.6
12.6
11.3
11 0
16.9
8.9
9.6
12.2
11.0
Corr.
~oeff.~
-
No. of
samples
CV of
body wtC
Trend
body wtd
17
9
18
11
35
16
21
15
15
11
46
15
27
18
11
0.49
0.42
0.19
0.29
0.51
0.4 1
0.36
0.21
0.47
0.18
0.40
0.31
0.49
0.30
0.21
0.36
0.26
0.85
0.32
0.19
0.73
0.27
0.23
0.25
No
No
No
No
No
No
No
No
No
Posit~ve
No
Negative
No
No
No
No
Positive
No
No
No
No
No
Positive
No
-
0.57'
0 35
0 39
0.6
0.55
0.87 '
0.70 '
0.95
0.47
0.79"
0.72"
0.57'
0.88"
0.56'
0.86"
0.82
0.62
0.63
0.67.
0.47'
0.52
0.70"
0.62
0.67"
m m
m
m m
18
16
49
41
18
18
17
18
12
bCorrelation coefficient ( ' s i g n ~ f ~ c a natt 5% and "at 1 % level). 'Coefficient of variation of yearly
a E x p o n e n t ~ acoefficient.
l
change of mean body weight. "Trend of yearly body weight
Mar Ecol Prog Ser 160: 109-120, 1997
118
0.00
1984
- - c-- - Mcan body kngth
1986
1988
1990
1992
1994
0
1996
Year
Fig. 10. Kareius bicoloratus. Yearly change of '37Cs concentration and mean body length of stone flounders
of size together with the size-dependent concentration
in this species (caused by change of food habits with
growth, Figs. 3 & 5).
Through our investigations of food habits it is possible to describe most of the concentration levels of '"CS
in surface fishes (those that inhabit the surface layers
a
m
Common conger
-
m
6
Bertail flathead
0
Japanese sea bass
Atka mackerel
I
Stone
, flounder
, ,
0
0
500
1
1000
Mean Body Weight (g)
,
0
Brown
, , , sole
,
500
1
l000
Mean Body Weight (g)
Fig 11 Relationship between weight of fish and S1'N (from
Kasamatsu et al. unpubl.). Muscle samples for SI5N were
frozen and 615N was measured using a Finnigan MAT Model
delta E , following the method described in Minagabva & Wada
(1984)
with a sea temperature of approximately 10 to 25°C);
however, we identified another group of fishes having
relatively high concentration levels of '37Cs despite a
low concentration in their food (e.g. walleye pollack,
Atka mackerel, and deep-sea smelt, all of which
inhabit deep-sea areas with a water temperature of
less than 3 to 5OC), indicating that concentrations of
'37Cs in these fishes could not be explained only
through their food habits. Kolehmainen et al. (1968)
and Cocchio et al. (1995) suggested a decrease of
excretion rate (increased biological half-lives) when
the difference of environmental temperature is more
than 10°C. Because there is no information on the
absorption rate of 137Csat low temperatures or in
changing temperatures, it is not possible at this stage
to make conclusions about factors affecting accumulation of 13'Cs in deep-sea fishes. However, it is reasonable to suggest that environmental conditions (e.g. sea
temperature) together with biological conditions (e.g
low food availability) may affect accumulation of '37Cs
in these fishes. Since there is little information on the
effect of depth of habitat (effect of temperature, difference of food or availability of food, etc.) on accumulation of radionuclides, especially for 13'Cs, this is a topic
that should be investigated further.
The natural variation of S'",
which has recently
been used to identify the trophic level of animals in
relation to their food habits or trophic levels (Owens
1987, Wada et al. 1987, Fry 1988), was examined and
its behavior compared in relation to food habits to that
of '''CS. Fig. 11 shows the relationship between body
weight and 615N in 10 fish species in which the '37Cs
concentration was also measured. In common Japanese conger, Pacific cod, bartail flathead and stone
flounder, which shift their food habits to a higher
trophic level with growth, '37Cs concentration shows
good agreement with the change of food habits
according to growth (Figs. 2 & 3) but 61SN does not
show a significant change with growth except Pacific
cod. Because the biological half-life of 13'Cs is relatively short (approximately 100 d ; Gomez et al. 1991),
concentration of 13'Cs in fishes may well reflect minor
changes in prey species or variation of food quantity
better than 615N.
Acknowledgements. We express our thanks to R. Saito, 1.
Ueda, Y. Nagaya, Y Suzuki. T Tomizawa, K. Yamada, N.
Nonaka, T. Iba, K. Marurno, S. Maeda. S. Sakamoto, H. Kawamura, K. Kawabe, T. Harasaki and N. Inatomi of our Institute
for their cooperation. We also express our thanks to P. Ensor
and B. Casareto for their superb editing. We thank 3 anonymous reviewers for their useful comments. The study could
not have been undertaken without the assistance and cooperation of the members of local fisherman's unions and the
Japan Chemlcal Analysis Center This study was conducted
as a part of a marine environmental radioactive monitoring
program by the Science and Technology Agency of Japan.
Kasamatsu & Ishikawa: Ii7Cs c:oncentrations in marine organisms
LITERATURE CITED
Baptist JP, Price TJ (1962) Accumulation and retention of
137Csby marine fishes. Fish Bull US 62:177-197
Bryan GW (1963) The accumulation of '"CS by brackish
water invertebrates and its retention to the regulation of
potassium and sodium. J Mar Biol Assoc UK 43:541-575
Bryan GW (1965) Ionic regulation in the squat lobster
Golathea sqamlfera, with special reference to the relationship between potassium metabolism a n d the accumulation of radioactive caesium. J Mar Biol Assoc UK 45:
97-113
Cocchio LA, Rodgers DW, Beamish FWH (1995) Effects of
water chem~stryand temperature on radiocesium dynamics in rainbow trout, Onchorhynchus mykiss. Can J Fish
Aquat Sci 52:607-613
Fry B (1988) Food web structure on Georges Bank from stable
C , N, and S isotopic composition. Limnol Oceanogr
33:1182-1190
Gomez LS, Marietta MG, Jackson DW (1991) Compilation of
selected marine radioecological data for the formerly
utilized sites remedial action program; summaries of available radioecolog~calconcentratlon factors and biological
half-lives. SAND89-1585-UC-721 Sandia National Laboratories, Livermore, CA
Gustafson PF (1967) Comments on radionuclides in aquatic
ecosystems. In: Aberg B. Hungate FP (eds) Radioecological concentration processes Pergamon Press, Oxford,
p 853-858
Hasanen E, Kolehmalnen S, Mietinen J (1968)Biological halftimes of '"CS and Z2Na in different fish spt!cies and
their temperature dependence. In: Snyder WS (ed) Proc
1st Int Congr of Radiation Protection. Pergamon Press,
Oxford, p 401-406
Hasanen E, M~ettinenJ (1963) Caesium-137 content of freshwater fish in Finland. Nature 200 1018-1019
Hiyama Y, S h i m ~ z uM (1964) On the concentration factors of
radioactive CS. Sr, Cd, Zn, and C e in marine organisms.
Rec Oceanogr Works J p n 7:43-77
lbaraki Environmental Pollution Research Center (1993)
Radioactivity survey in Ibaraki, No. 36
lbaraki Environmental Pollution Research Center (1994)
Radioactivity survey in Ibaraki, No. 37
lbaraki Environmental Pollution Research Center (1995)
Radioactivity survey in Ibaraki, No. 38
Ishikawa Y, Yamada K, Nonaka N. Marumo K, Ueda T (1995)
Size-dependent concentrations of radiocesium and stable
elements in muscles of flathead flounder Hippoglossoides
dubius. Fish Sci (Tokyo) 61:981-985
Jefferies DF, Hewett CP (1971) The accumulation and excretion of radioactive caesium by the pla.ice (Pleuronectes
platessa) and the thornback ray (Raja clavata). J Mar Biol
Assoc UK 51:411-422
Kasamatsu F (1996) Notes o n possible change in the food of
atka mackerel, Pleurogrammus azonus, taken off Niigata,
as suggested by recent change of radiocesium concentrations. Bull J a p Soc Fish Oceanogr 60:227-236 (in Japanese
with English abstract)
Kasamatsu F, Inatomi Y (1997) Effective environmental halflife of "Sr and '37Cs in the coastal seawaters of J a p a n .
J Geophys Res (in press)
Kimura K (1984) Accumulation a n d retention of cesium-137
by the common goby. Bull J a p Soc Sci Fish 50:481-487
King SF (1964) Uptake and transfer of cesium-l37 by
Chamidomonas, Daphnia, and bluegill fingerlings Ecology 5:852-859
Kolehmainen SE (1974) Daily feeding rates of bluegill
119
(Lepomjs macrochil-us) determined by a refined radio~ s o t o p emethod. J Fish Res Bd C a n 31 67-74
Kolehmainen SE, Hasanen E, Miettinen J (1968) '"CS in the
plants, plankton, a n d fish of Finnish lakes and factors
affecting its accumulation. In: Snyder WS (ed) Proc 1st Int
Congr of Radiation Protection. Pergamon Press, Oxford.
p 407-415
Mallhot H , Peters RH, Cornett RJ (19881 Bioaccumulation of
cesium by aquatic organisms. Int Ver Theor Angerv
L~mnolVerh 23:1602-1609
Minagawa M. Wada E (1984) Stepwise enrichment of I5N
along food chain: further evidence and the relation
between 6''N a n d animal age. Geochem Cosmochim Acta
48:1135-1140
Morgan F (1964) The uptake of radioactivity by f ~ s hand shellfish. 1 Caesium-134 by whole animals J Mar Biol Assoc
UK 44:259-271
Morgan IJ, Tytler P, Bell MV (1993) T h e accumulation of 137cesium from fresh water by alevins and fry of Atlantic
salmon and brown trout. J Fish Biol43:877-888
Morita S (1980) Accumulation and metabolism of radionuclides: Fishes. In: B~ologicalconcentratlon in the ocean
and factors affecting it. National Institute of Radlologlcal Science, Science and Technology Agency, Tokyo,
p 139-146
Newman MC, Brisbin IL J r (1990) Variation of I3'Cs levels
between sex, body size and collection localities of mosquitofish, Gambusia holbrooki (Girard 1859), inhabiting
reactor cooling reservoir J Environ Radioact 12:131-141
Owens NJP (1987) Natural vanations in "N in the marine
environment. Adv Mar B101 24:389-451
Pendleton RC, Mays CW, Lloyd RD, Hurch BWC (1965) A
trophic level effect on caesium-137 concentrations. Health
Physics 11:1503-1510
Pentreath RJ (1973) T h e role of food and water in the accumulation of radionuclides by marine teleost and elasmobranch fish. In: Radioactive contamination of the marine
environment. IAEA, Vienna, p 421-436
Pentreath RJ, Jefferies DF (1971) The accumulation of radionuclides by I-group plaice (Pleuronectes platessa) off
the Cumberland coast, Irish Sea. J Mar Biol Assoc UK 51:
963-976
Reichle DE (1969) Measurement of elemental assimilation by
anlmals from radioisotope retention patterns. Ecology 501102-1104
Reichle DE. Dunaway PB. Nelson DJ (1970) Turnover and
concentration of radionuclides in food chains. Nucl Saf
11:43-55
Rowan DJ, Rasmussen JB (1994) Bioaccumulation of radiocesiuin by fish: the influence of physicochemical factors
and trophic structure Can J Fish Aquat Sci 51:2388-2410
Suzuki Y, Nakamura R, Ueda T (1973) Cesiuin-l37 contamination of marine f ~ s h e sfrom the coast of J a p a n . J Radiat
Res 14:382-391
Tateda Y. Misonou J (1991) T h e ecological half-life of Cs137 in Japanese coastal marine biota. In: Kershaw
PJ, Woodhead DS (eds) Radionuclides in the study of
marine processes Elsevier Applied Science, London,
p 340-349
Thomann RV (1981) Equilibrium model of fate of rnicrocontaminants in diverse aquatic food chains. Can J Fish Aquat
Res Sci 38:280-296
Wada E, Terasaki M, Kabaya Y, Nemoto T (1987) 615N a n d
6I3C abundances in the Antarctic Ocean with emphasis o n
the biogeochemical structure of the food web. Deep Sea
Res 34.829-841
W h ~ c k e rFW, Nelson WC, Gallegos AF (1972) Fallout '37Cs
120
Mar Ecol Prog Ser 160: 109-120. 1997
a n d '"'Sr in trout from mountain lakes in Colorado. l.lealth
Physics 23:519-527
PVilliams LG, P ~ c k e n n g Q (1961) Dirpcl a n d food-chain
uptake of cesium-137 dnd stront~um-90In bl.uegil1 fingerlings. Ecology 42:205-206
Yosh~daK (19921 Distribution and radioact~vltyof deep-sea
macrourids in waters around Izu-Ogasrturard Trench. In:
Thc 34th Env~ronmentalRadioactivity Research and Survcy Reports. Science and Technology Agency, Tokyo, p
49 -50 ( ~ Japanese)
n
Editorial respons~bility.Otto K ~ n n e(Editor),
Oldendorf/Luhe, Germany
Subm~tled.June 13. 1997; Accepted: September 29, 1997
Proofs recelved from author(s):December 2, 1997